Developing a gateway program for importing non‐animal origin ingredients from regions with African swine fever virus

Abstract The US Department of Agriculture (USDA) categorizes the risk of African swine fever virus (ASFV) entry into the United States through non‐animal origin feed ingredients as ‘negligible to moderate, with high uncertainty’. Both Canada and Australia have implemented policies that are suggested to reduce the risk of ASFV entry through feed ingredients, but the United States has not because of scientific limitations that have been addressed by recent publications. As regulators and industry consider a potential pathway forward, the objective of this manuscript is to describe a process to determine if a voluntary or regulatory import policy is warranted by the United States. Initially, the volume and types of non‐animal origin feed ingredients imported from countries with ASFV were quantified and assigned a level of risk (high risk: unprocessed grains and oilseeds, moderate risk: soybean co‐products (meals, oil, and oilcake), and low risk: amino acids, vitamins, and other synthetically produced products from countries that have ASFV). In 2020, moderate‐ and high‐risk ingredients from ASFV‐positive countries represented 3.1% of all ingredients imported into the United States. Policies from Canada and Australia were evaluated for practicality of implementation by US government officials. Industry representatives from both countries consistently stated their policies would not be feasible in the United States due to the differences in cost and complexity of the swine and feed industries. Overall, unprocessed, or high‐risk, ingredients from ASFV‐positive countries represent a low percentage of imported ingredients into the United States; however, cautionary procedures may still be warranted given industry demand.


INTRODUCTION
Currently, African Swine Fever virus (ASFV) has been confirmed in pigs in more than 50 countries. As the number of affected countries grows, so does the risk for virus entry into the United States. The most likely method of ASFV transmission is direct contact between pigs. In countries free from disease, prevention of entry is focused on preventing fomite-based transmission. One potential route for fomitebased transmission is the feed supply chain. The USDA cites that used tote bags carrying feed ingredients was the most likely source of porcine epidemic diarrhoea virus (PEDV) entry into the United States from China in 2013 (USDA-APHIS, 2015). The virus was then spread throughout North America and remains endemic throughout the continent today. Research has shown that feed ingredients have the capability to sustain not only PEDV, but a host of other viruses, including ASFV (Dee et al., 2018).
In order for a feed ingredient to serve as a fomite in disease transmission, it must first be contaminated by the pathogen, that pathogen must survive transport to the point of consumption by an animal, and the quantity of virus consumed by an animal must be substantial enough to cause disease. These factors can vary widely in different types of ingredients. For example, wild boar or feral pigs affected by ASFV often seek food and shelter in fields. Their resulting carcasses may contaminate grains or seeds during harvest. Due to these differences, unprocessed grains or seeds from ASFV-endemic regions are considered to be at a greater risk to be contaminated with the pathogen than manufactured ingredients, such as synthetic amino acids or vitamins, derived from the same region (EFSA, 2021). Virus survival also differs based on ingredient type. For example, the half-life of ASFV can range from 9.6 to 12.9 days in conventional versus organic soybean meal . Research has demonstrated that if ingredients are contaminated with a high level of ASFV, the virus can survive theoretical trans-oceanic shipment to the United States (Dee et al., 2018). Finally, feed contaminated with ASFV has been demonstrated to cause infection in pigs when sufficient quantities of virus are ingested .
These studies have raised concern that the feed supply chain may be a realistic route of ASFV entry into the United States. Both Canada and Australia have regulations to reduce this risk. Scientific limitations have slowed the implementation of similar rules in the United States.
For example, there are no approved sampling or extraction protocols for ASFV detection in ingredients. Recent publications have helped to address these issues, and while some challenges still remain, there is greater confidence that a representative sample can be collected and analysed for ASFV if testing were allowed (Dee et al., 2021;Jones et al., 2019). This scientific progress led to the US Animal Health Association passing a resolution in 2020 that requested the federal government to 'restrict the import of feed and/or a feed ingredient from countries that are positive for African swine fever and to create enforceable standards for those countries to reduce the contamination threat during harvest and processing of the feed and feed ingredients' . However, the government responded that there is too great of cost to both government and industry at the current time to implement such a program.
Furthermore, the types of enforceable standards requested were too broad; there are mixed messages from within both the swine and feed industries about the types of standards that should be implemented.
As regulators and industry consider a potential pathway forward, the objective of this manuscript is to describe a process to determine if a voluntary or regulatory import policy is warranted by the United States.

MATERIALS AND METHODS
To make the determination if an industrywide policy should be adopted, and what it should address, it was important to first quantify the sources and volumes of non-animal origin ingredients imported into the United States from ASFV-positive regions. Next, an assessment of the regulatory framework incorporated by other ASFV-free countries was considered. Finally, a working group representing the swine industry made recommendations for a pilot import program and its eventual incorporation into regulatory policy.

2.1
The volume and path of non-animal origin feed and ingredients imported from countries with ASFV Import data from 2016 through 2020 were collected from the US International Trade Commission (USITC DataWeb) with the Harmonized Tariff Schedule (HTS) found in Table 1. Disease presence was based off OIE-World Organization for Animal Health (OIE-WAHIS) disease reporting database. Imported ingredients were separated into three categories based off their perceived risk of contamination or re-contamination upon importation into the United States (Table 2).
'Low-risk' ingredients were those that were least likely to be contaminated with ASFV, such as ingredients that are synthetically manufactured (amino acids, vitamins, enzymes) or undergo substantial thermal or chemical processing that would likely render pathogen inactive (oils and most oilseed cakes or flours). 'Moderate-risk' ingredients were those that undergo thermal or chemical processing, but allow for the risk of post-processing cross-contamination and demonstrate a capacity for significant viral survival over time (soybean oilcake and soybean meal). 'High-risk' ingredients were those that have a risk for natural contamination by affected animals and undergo minimal processing (whole grains or seeds). Notably, an exception was made to also characterize choline as a 'high-risk' ingredient. Similar to vitamins, the synthetic production of choline poses little risk for ASFV contamination. While most vitamins are transported to the United States in their highly concentrated form and diluted upon arrival to the United States, choline is typically applied to a corncob or rice hull carrier shortly after manufacturing because it is highly hygroscopic. This application maximizes its stability during transoceanic shipment. The carrier to which choline applies has a similar probability of contamination as whole grains or seeds, so the imported product category of choline was included in the 'high-risk' category.

Current regulations for non-animal origin feed and ingredients imported from ASFV-positive regions
To understand the complex environment of importation requirements across three countries, the guidelines from the United States, Canada and Australia were initially reviewed. Canada and Australia were selected for comparison because, similar to the United States, they are countries free from ASFV but depend on imports from ASFV-positive countries. They also had implemented significant policies to prevent disease entry through ingredients. Independent interviews were also conducted with representatives in each country representing the federal government, feed industry and swine industry. Positions

The volume and path of non-animal origin feed and ingredients imported from countries with ASFV
From 2016 to 2020, the quantity of feed ingredients imported into the United States ranged from 11.6 to 12.8 million metric tons per year ( Figure 1). This quantity does not differentiate between those ingredients intended for human consumption, swine diets or other livestock and pet food diets. During the same time frame, the total quantity imported from ASFV-positive countries ranged from 0.8 to 1.1 million metric tons per year. The greatest quantity imported from ASFVpositive countries was in 2020, with the increase from recent years due to the growing number of United States' trade partners that were impacted by the disease. In 2020, the United States imported ingredients that could be used in swine feed from 29 of the 50 countries that were ASFV-positive, some of which are critical to US trade (Figure 2).
The greatest quantity of high-risk imported ingredients came from Germany, with all the incoming product consisting of grains. Relatively significant quantities of soybeans were imported from Russia, Ukraine and India in 2020, as well as grains from Romania. Choline was largely sourced from Belgium. Notably, fewer than 5000 metric tons of high-risk ingredients were imported from China in 2020. These high-risk ingredients were imported into 23 different US ports (Figure 3).
The Port at New Orleans imported the greatest quantity of high-risk ingredients from ASFV-positive countries at more than 114,000 metric tons of product. These shipments contained 9 metric tons of barley imported from Italy and likely destined for human food and 114,775 metric tons of certified organic soybeans from Ethiopia, Russia, and Ukraine (Table 3). The source of these ingredients (i.e. region of a specific country) and transportation methods could not be further determined prior to their Port of Loading. Interestingly, the Ports of Loading for these shipments were from India and Turkey. This demonstrates that even when a country of origin can be determined for an ingredient, its growing conditions, transportation and other factors relating to the likelihood of ASFV contamination is unlikely to be known. These three shipments arrived at the Port of New Orleans in jumbo bags (45) or bulk (1) consignments after at least 32.4 days at sea. Part or all of each shipment was purchased by a single company, Sunrise Foods International, an entity based in Canada. These soybeans would likely require crushing prior to use in swine diets because whole, unprocessed soybeans have poorly available nutrients to pigs (Liener, 1994). Therefore, it is unlikely that any of the high-risk ingredients received into the Port of New Orleans in 2020, which represents 31.4% of all high-risk ingredients imported, was consumed by pigs. Moreover, it is improbable that the remaining high-risk ingredients imported into other ports in 2020 were consumed by pigs due to the small volume of each consignment.
For example, the Port of New York had the greatest number of consignments, or individual shipments of high-risk ingredients. However, these consignments totalled to fewer than 14,000 metric tons of product, with most of the product arriving in small quantities that would be unlikely to be destined for animal feed.

Canada
Canada developed their risk management strategy based on the concept of strengthening the country's protection against ASFV entry in ingredients, but not eliminating the risk altogether. Their import policy was implemented after an extensive literature review and importer surveys to better understand the number of importers affected and their understanding of pathogen transmission in feed. Canada requires an import permit for any raw or unprocessed grains and oilseeds and any plant-based meal of concern imported from an ASFVpositive country. They also recognize regionalization with 12 countries.
Regionalization is permitted in countries who participate in the Euro- however, no analysis has been conducted to better understand the economic difference since this program has been implemented. All Canadian representatives stated that they did not believe a policy similar to Canada's would be practical to implement in the United States due to the greater complexity of grain trade and marine ports that exist in the United States.

Australia
Australia implemented import control measures approximately 20 years ago to reduce the risk of introducing foot and mouth disease virus, bovine spongiform encephalopathy and plant pests, such as the Khapra beetle. After ASFV was identified in Southeast Asia, the Australian Department of Agriculture reviewed their policies and confirmed their existing rules would effectively prevent ASFV entry in ingredients so no new policies were needed. Current policies include that all imported cereal grains and oilseeds must be either processed at the port of entry or have an import permit from the country of origin signed by a competent authority that the product was effectively processed. All foreign facilities that process ingredients bound for Australia must be audited by the Australian government every 2 years at the cost to the importing facility (∼$10,000 AUD/audit).
Accepted processing methods include (1) heating the product to a core temperature of 85 • C for 10 min if it originates from a low-risk country or to 100 • C for 30 min if it originates from a high-risk country; (2) pH reduction by 3.3 or (3) irradiation of 50 kGy. Australian pork industry officials interviewed described that even with these import restrictions in place, they frequently implemented their own holding time mitigation strategies due to their lack of confidence in effective processing by importing countries. The Australian government is currently conducting a cost:benefit analysis to determine the value of mitigation strategies to prevent ASFV. However, their analysis does not consider the role of feed or ingredients as a vector of ASFV entry or transmission. All Australian representatives stated that they did not believe a policy similar to Australia's would be practical to implement in the United States due to the size of the US feed and pork industries. In fact, both regulators and industry representatives alike expressed their concern that existing policies reduced

LIMITATIONS
As with any study, there are limitations which must be addressed. Due to time restraints, a limited number of individuals were able to be interviewed. As the objectives were primarily focused on regulatory struc-ture in certain countries, the interviews primarily focused on governing regulatory bodies and national organizations. This limited representation from individual swine producers and veterinarians, which may view the challenges facing the swine industry differently than those interviewed.

CONCLUSION
There continues to be a small, but realistic threat for African swine fever virus entry into the United States through non-animal origin feed ingredients. In 2020, moderate-and high-risk ingredients from ASFVpositive countries represented only 3.1% of all ingredients imported into the United States. While the United States has policies to prevent foreign entry of plant pests and diseases, Canada and Australia have been more aggressive in their regulatory approach to prevent animal pathogens in plant-based ingredients. Industry led practices can be developed to disallow use of high-and medium-risk ingredients from ASFV-positive countries in swine feeds and require the use of mitigation strategies in low-risk ingredients if there is a high demand from producers and industry leaders.

ACKNOWLEDGEMENT
This project was funded by the National Pork Board and the National Pork Producers Council, Ames, IA.

CONFLICT OF INTEREST
The authors declare no conflicts of interest in the completion and reporting of results for this investigation.

DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from corresponding author upon reasonable request.